Download Plant Nutrition: Root Transporters on the Move

Update on Nutrient Transporters
Plant Nutrition: Root Transporters on the Move1
Enric Zelazny and Grégory Vert*
Institut des Sciences du Végétal, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2355,
Saclay Plant Sciences, 91190 Gif-sur-Yvette, France
Nutrient and water uptake from the soil is essential for plant growth and development. In the root, absorption and radial
transport of nutrients and water toward the vascular tissues is achieved by a battery of specialized transporters and channels.
Modulating the amount and the localization of these membrane transport proteins appears as a way to drive their activity and is
essential to maintain nutrient homeostasis in plants. This control first involves the delivery of newly synthesized proteins to the
plasma membrane by establishing check points along the secretory pathway, especially during the export from the endoplasmic
reticulum. Plasma membrane-localized transport proteins are internalized through endocytosis followed by recycling to the cell
surface or targeting to the vacuole for degradation, hence constituting another layer of control. These intricate mechanisms are
often regulated by nutrient availability, stresses, and endogenous cues, allowing plants to rapidly adjust to their environment
and adapt their development.
Plants take up nutrients and water from the soil
and transport them to the leaves to support photosynthesis and plant growth. However, most soils
around the world do not provide optimal conditions
for plant colonization. Consequently, plants have
evolved sophisticated mechanisms to adjust to deficiency or excess of nutrients and water supply.
Membrane transport proteins, including channels
and transporters, play crucial roles in the uptake of
nutrients and water from the soil and in their radial
transport to the root vasculature. Newly synthesized
membrane transport proteins have to be properly
targeted to a defined compartment, usually the plasma membrane, to efficiently ensure their function. The
trafficking of membrane transport proteins along the
secretory pathway is tightly controlled and involves the
recognition of exit signals by gatekeeper protein complexes. After reaching the plasma membrane, membrane transport proteins can be endocytosed and
subsequently recycled to the cell surface or targeted
to the vacuole for degradation. Because the subcellular localization of proteins directly influences their
activity, modulating the localization of membrane
transport proteins constitutes a powerful way to
control nutrient and water uptake in plants. This
review discusses the fundamental mechanisms at
stake in membrane protein secretion and endocytosis, with a specific focus on membrane transport
proteins, and how endogenous and exogenous cues
affect their dynamics to integrate uptake of nutrients and water to plant growth conditions.
1
This work was supported by the Agence Nationale de la
Recherche (grant no. ANR–13–JSV2–0004–01 to G.V.) and the European Commission Marie Curie Actions Fellowship Program (grant
no. PCIG12–GA–2012–334021 to G.V.).
* Address correspondence to [email protected].
www.plantphysiol.org/cgi/doi/10.1104/pp.114.244475
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GENERAL PRINCIPLES OF MEMBRANE PROTEIN
TRAFFICKING THROUGH THE SECRETORY AND
ENDOCYTIC PATHWAYS
Transport between the Endoplasmic Reticulum and the
Plasma Membrane
The endoplasmic reticulum (ER) is the departure point
of the secretory pathway where synthesis, folding, disulfide bond formation, and oligomerization of the proteins take place. Misfolded proteins are selected by the
endoplasmic reticulum-associated degradation (ERAD)
machinery and retrotranslocated into the cytosol for
ubiquitin/proteasome-mediated degradation (Guerra
and Callis, 2012). On the other hand, functional proteins
are exported from the ER using vesicles coated with coat
protein complex II (COPII) that is composed of three
cytosolic components: the GTPase Sar-1, Sec23/Sec24,
and Sec13/Sec31 heteromers (Barlowe et al., 1994;
Aridor et al., 2001). Recruitment of cargo proteins in
COPII vesicles is mediated by Sec24. Thus far, multiple
independent cargo binding sites recognizing diverse
ER sorting signals, such as diacidic motifs, have been
identified on Sec24 (Miller et al., 2003; Mossessova et al.,
2003). Diacidic motifs correspond to the (D/E)x(D/E)
sequence, where x represents any amino acid, and are
functionally conserved from virus to animals (Nishimura
and Balch, 1997; Zuzarte et al., 2007). Although the role
of the COPII complex was mostly investigated in yeast
(Saccharomyces cerevisiae) and mammals, several studies
highlighted that the COPII machinery is conserved in
plants and is responsible for protein export from the ER
(Mikosch et al., 2006; Takagi et al., 2013).
In parallel to the anterograde route mediated by
COPII, a retrograde pathway is operated by vesicles
coated with COPI, which allow the continual recycling
of proteins and lipids from the Golgi to the ER in order
to maintain an equilibrium with COPII transport. Although COPI-mediated transport was mostly studied
in yeast and mammals, the presence of homologs of
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Nutrient Transporter Dynamics
COPI proteins in plants suggested that the function
of this complex was conserved and COPI-containing
vesicles were identified (Contreras et al., 2000; Pimpl
et al., 2000).
The Golgi apparatus has a major role in sorting proteins toward other cellular compartments including the
plasma membrane and the vacuole. In plants, the Golgi is
involved in the synthesis and the assembly of complex
polysaccharides of the cell wall and in the production of
glycolipids for the plasma membrane and the tonoplast.
The Golgi is composed of individual cisternae and is
subdivided into three parts, the cis-, medial-, and transGolgi, which make this organelle polarized (Hwang and
Robinson, 2009). Proteins coming from the ER arrive
first in the cis-Golgi and then pass sequentially in the
two other compartments, finally reaching the trans-Golgi
network (TGN) that in plants exists as an independent
organelle from the Golgi (Brandizzi and Barlowe, 2013).
Vesicles coming from the TGN lastly fuse with the plasma membrane to deliver the cargo proteins.
The Endocytic Pathway from the Cell Surface to
the Vacuole
Plasma membrane proteins can be internalized using
clathrin-dependent or clathrin-independent pathways.
Clathrin-mediated endocytosis (CME) initiates at specific foci of the plasma membrane called clathrin-coated
pits by the recruitment of the heterotetrameric adaptor
protein2 complex and the hexameric clathrin complex
(Chen et al., 2011a; Baisa et al., 2013). Along with the
formation of the clathrin cage, clathrin-coated pits mature into clathrin-coated vesicles that will be released
from the plasma membrane. In plants, key components
of the CME machinery are conserved, and our knowledge of CME mechanisms increased considerably in
recent years (Chen et al., 2011a; Baisa et al., 2013). A
crucial step in CME is the selection of cargo proteins in
clathrin-coated vesicles via the recognition of specific
sorting signals. Subunits of the Adaptor Protein2 complex select cargo proteins by recognizing di-Leu motifs
[DE]xxx[LIM] (x is any amino acid) and Tyr-based
motifs YxxF (F is a bulky hydrophobic amino acid;
Traub, 2009). Ubiquitination, a posttranslational modification in which the 76-amino acid polypeptide ubiquitin
is attached onto a Lys residue of a protein, is also recognized by the CME machinery and plays a crucial role
in cargo internalization from the plasma membrane
(Lauwers et al., 2010). Importantly, CME is not the only
way membrane proteins are internalized. The Arabidopsis
(Arabidopsis thaliana) membrane microdomain-associated
protein Flotillin1 was recently associated with clathrinindependent endocytosis (Li et al., 2012), as previously
demonstrated in mammals (Hansen and Nichols, 2009).
After internalization, membrane proteins are targeted
to early endosomes (EEs). In plants, EEs have been
demonstrated to coincide with the TGN in the early
endosome/trans-Golgi network (EE/TGN; Dettmer
et al., 2006) and may contain specialized subdomains
with secretory or endocytic functions (Contento and
Bassham, 2012). From the EE/TGN, membrane proteins
can be recycled to the plasma membrane, which involves
vesicle budding regulators named ADP ribosylation
factor-guanine nucleotide exchange factor (ARF-GEF)
proteins (e.g. GNOM) that are sensitive to the toxin
brefeldin A (BFA; Geldner et al., 2003). By inhibiting
ARF-GEF activity, BFA triggers the accumulation of
endocytosed protein in large bodies in plant roots,
making this drug a very interesting tool to study endocytosis and recycling. Alternatively, endocytosed
transporters are targeted to late endosomes named
multivesicular bodies (MVBs) that constitute an intermediate compartment before the vacuole where protein degradation occurs. Ubiquitination is known to
play a critical role in MVB sorting (MacGurn et al.,
2012). The endosomal sorting complex for transport
(ESCRT), composed of four subcomplexes (ESCRT-0 to
ESCRT-III), captures ubiquitinated cargos in the endosome membrane and allows their sorting in intraluminal
vesicles of the MVB and subsequent vacuolar/lysosomal
targeting (Henne et al., 2011). Most of the ESCRT proteins
identified in yeast and mammals are conserved in plants,
except a canonical ESCRT-0 subcomplex whose role is to
initially recognize and concentrate ubiquitinated cargos
(Leung et al., 2008). However, Arabidopsis proteins
related to Target of Myb1 were recently proposed to
compensate for the absence of ESCRT-0 by functioning as early gating factors for recognition and sorting
of ubiquitinated cargos (Korbei et al., 2013). Interestingly, deubiquitination of cargos by the action of
deubiquitinating enzymes was proposed to promote
the recycling of ubiquitinated substrates at an early
stage of the endosomal sorting process, and hence to
rescue these cargos from degradation (Bomberger et al.,
2009). At late steps of endocytosis, cargo proteins can
be retrieved to earlier endocytic compartments by the
retromer complex (for review, see Seaman, 2012). In
mammals, the retromer is composed of two subcomplexes:
the core retromer constituted by Vacuolar Protein Sorting
(VPS)26, VPS29, and VPS35 and a dimer of Sorting Nexin
(SNX; Seaman, 2012). In Arabidopsis, all members of the
retromer are conserved; however, recent data suggest
that the core retromer and the SNX dimer probably behave as independent units (Jaillais et al., 2007; Pourcher
et al., 2010; Zelazny et al., 2013). Even if the subcellular
localization of the plant retromer is still a matter of debate, this complex was shown to primarily localize in
Ara7/RabF2b-positive MVBs (Jaillais et al., 2007).
SECRETION OF PLANT MEMBRANE
TRANSPORT PROTEINS
Thus far, the mechanisms by which plant membrane
transport proteins travel along the secretory pathway
have been poorly studied. In this section, we present
the knowledge gained over the past few years on membrane transport protein exit from the ER and targeting to
the plasma membrane.
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Zelazny and Vert
Export from the ER
The role of diacidic motifs in the ER export of membrane transport proteins in plants is well illustrated by
the water channels aquaporins. Some Plasma membrane
Intrinsic Protein2 (PIP2) proteins from Arabidopsis and
maize (Zea mays) carry in their N-terminal part a DxE
motif that has been demonstrated by mutation analyses
to be essential for ER exit (Fig. 1; Zelazny et al., 2009;
Sorieul et al., 2011). Extensive work in yeast and mammals demonstrated that diacidic motifs are recognized
by the Sec24 protein from the COPII complex (Miller
et al., 2003; Mossessova et al., 2003). This recognition
seems to be conserved in plants because the Arabidopsis
potassium channel KAT1 is recruited into COPII vesicles
via binding of a diacidic motif to Sec24 (Sieben et al.,
2008). Interestingly, in Arabidopsis roots, overexpression
of AtPIP2;1 mutated in the diacidic export motif induced
a strong reduction in the root hydraulic conductivity
compared with wild-type plants (Sorieul et al., 2011).
Because aquaporins form tetramers, it was proposed that
the mutated AtPIP2;1 interacts with endogenous PIPs
and induces ER retention of the complex, leading to a
decrease in PIP levels at the cell surface. Heteromerization
between PIP1 and PIP2 proteins, which constitute two
groups of PIPs with different properties, appears as a
way to control their ER export. When expressed alone
in maize cells, ZmPIP1 proteins are retained in the ER,
whereas ZmPIP2 proteins are targeted to the plasma
membrane (Zelazny et al., 2007). However, upon heteromerization with ZmPIP2s, ZmPIP1s are efficiently
addressed to the plasma membrane, suggesting that
ZmPIP2s provide export signals that are sufficient to
overcome the ER retention capacity of ZmPIP1s.
Posttranslational modifications, such as ubiquitination,
constitute important signals regulating the fate of membrane proteins. In Arabidopsis, overexpression of the ER
resident E3 ubiquitin ligase Ring membrane-anchor1 H1
(Rma1H1) decreases PIP2;1 levels and inhibits its trafficking from the ER to the plasma membrane, concomitantly conferring enhanced tolerance to drought stress
(Lee et al., 2009). Rma1H1 was shown to ubiquitinate
PIP2;1, likely leading to its degradation by the proteasome.
Because Rma1H1 expression is induced by stresses such
as dehydration (Lee et al., 2009), the enhanced degradation of PIP2;1 at the ER level might result from an
ERAD- degradation process of PIP2;1. Phosphorylation
has been also demonstrated to control ER export of
membrane transport proteins. Mutation of a C-terminal
Ser to the phosphomimic Asp in the Arabidopsis Phosphate Transporter1;1 (PHT1;1) leads to ER retention,
suggesting that phosphorylation prevents PHT1;1 exit
from the ER in root cells (Fig. 2A; Bayle et al., 2011).
Interestingly, phosphorylation plays an opposite effect
in the trafficking of some Arabidopsis aquaporin. PIP2;1
is phosphorylated on Ser283 and mutation of this residue to Ala triggers a strong retention of PIP2;1 in the ER
(Prak et al., 2008).
In yeast, the first step in COPII vesicle formation
required the Sec12 protein, a guanine nucleotideexchange factor (Barlowe and Schekman, 1993). Interestingly, mutation of the Arabidopsis ER-localized and
Sec12-related Phosphate Transporter Traffic Facilitator1
(PHF1) impairs ER exit of PHT1;1 and inorganic phosphate (Pi) uptake, without modifying the localization of
other plasma membrane proteins. This argues for a
specific action of PHF1 on Pi transporters (González
et al., 2005). Interestingly, the importance of PHF1 in the
ER exit of PHT1 proteins has also been demonstrated in
rice (Oryza sativa), suggesting a conserved mechanism
in plants (Chen et al., 2011b).
From the Golgi Apparatus to the Plasma Membrane
Figure 1. Diagram illustrating the constitutive dynamics of PIP2;1 in
Arabidopsis root cells. CIE, Clathrin-independent endocytosis; PM,
plasma membrane.
The mechanisms involved in the trafficking of membrane transport proteins between the Golgi apparatus
and the plasma membrane are still poorly understood in
plants. En route to the cell surface, Arabidopsis PHT1;1
and maize PIP2;5 have been demonstrated to partially colocalize with Golgi markers (Bayle et al.,
2011; Hachez et al., 2013). The post-Golgi trafficking
of ZmPIP2;5 was recently demonstrated to be regulated by the plasma membrane-localized soluble
N-ethylmaleimide-sensitive-factor attachment protein
receptor SYP121 known to regulate vesicular fusion
(Besserer et al., 2012). SYP121 and ZmPIP2;5 physically
interact and expression of the dominant-negative fragment of SYP121-Sp2 decreases the delivery of ZmPIP2;5
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Nutrient Transporter Dynamics
Figure 2. Diagram illustrating the substrateregulated trafficking pathways of PHT1 (A),
IRT1 (B), and BOR1 (C) in Arabidopsis root
cells. The putative secretory pathways of IRT1
(B) and BOR1 (C) are indicated by dashed oval
structures. Putative pathways are indicated by
dashed arrows. Note that in A, ubiquitination
of PHT1 in the ER requires the ubiquitinconjugating E2 phosphate2 enzyme (PHO2)
but also an unknown E3 ubiquitin ligase.
B, Boron; Co, cobalt; Mn, manganese; Zn, zinc;
PM, plasma membrane.
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Zelazny and Vert
to the plasma membrane. As a result, ZmPIP2;5 water
channel activity is negatively regulated by SYP121-Sp2
when expressed in protoplasts (Besserer et al., 2012). In
addition, SYP121 regulates the delivery of plant potassium channels (Sutter et al., 2006). A fluorescent imagingbased genetic screen recently identified BFA-visualized
exocytic trafficking defective5 (bex5) as a novel dominant
mutant defective in the exocytosis of PIPs. BEX5 encodes
the EE/TGN-localized RabA1b protein that plays a role in
protein trafficking between the EE/TGN and the plasma
membrane in Arabidopsis roots, probably by regulating
vesicle formation (Feraru et al., 2012).
Although most of membrane transport proteins pass
though the Golgi apparatus on their way to the plasma
membrane, some are residents of the Golgi such
as the Arabidopsis Metal Tolerance Protein11 (MTP11)
manganese transporter (Peiter et al., 2007). MTP11 was
proposed to allow the sequestration of manganese
excess into vesicles that traffic to the plasma membrane to release manganese from the cell via exocytosis. Interestingly, the Arabidopsis Ca2+/Mn2+ pump
endomembrane-type CA-ATPase3 has also been proposed to localize in the Golgi and to possibly transport
calcium and manganese into this organelle (Mills et al.,
2008). However, the localization of endomembranetype CA-ATPase3 remains unclear because this protein
was subsequently shown to localize in Ara7/RabF2bpositive late endosomes, where it might play a role in
manganese detoxification (Li et al., 2008).
ENDOCYTOSIS AND DEGRADATION OF
MEMBRANE TRANSPORT PROTEINS
Mechanisms of Internalization and Recycling from
the EE/TGN
CME is the major mechanism of endocytosis in
plants (Dhonukshe et al., 2007). Tyrphostin A23
(TyrA23), which impairs the recognition of YxxF
motifs by the CME machinery, inhibits the endocytosis
of the iron transporter IRT1, the ammonium transporter AMT1;3, and the aquaporin PIP2;1, indicating
that these membrane transport proteins undergo CME
(Dhonukshe et al., 2007; Barberon et al., 2011; Li et al.,
2011; Wang et al., 2013). CME of PIP2;1 and IRT1 was
confirmed by the use of a dominant-negative form of
clathrin (Dhonukshe et al., 2007; Barberon et al., 2014).
In root epidermal cells, IRT1 localizes in the EE/TGN
but rapidly cycles with the cell surface (Fig. 2B), as
revealed by TyrA23 treatment (Barberon et al., 2011).
IRT1 transports not only iron, but also highly reactive
manganese, zinc, and cobalt ions (Vert et al., 2002).
Therefore, limiting the plasma membrane pool of IRT1
by an internalization/recycling process appears as a
protective mechanism to limit the absorption of potentially toxic substrates (Zelazny et al., 2011).
Ubiquitination emerges as an essential signal driving
transporter endocytosis (Lauwers et al., 2010). In plants,
the dynamics of IRT1 between the cell surface and the
EE/TGN is dependent on its multi-monoubiquitination
on cytosol-exposed Lys residues (Barberon et al., 2011),
a process likely mediated by the E3 ubiquitin ligase
IRT1 DEGRADATION FACTOR1 (Shin et al., 2013).
The ubiquitination-defective IRT1K154RK179R mutant version
accumulates at the plasma membrane (Barberon et al.,
2011) and recent evidence point to a defect in internalization rather than to a mis-sorting in the MVB and subsequent recycling to the plasma membrane (M. Barberon
and G. Vert, unpublished data). Transgenic plants expressing nonubiquitinatable IRT1K154RK179R show severe growth defects due to uncontrolled metal uptake
(Barberon et al., 2011, 2014). Ubiquitination of phosphate
transporters has also been proposed to control their internalization from the plasma membrane. The E3 ubiquitin ligase NITROGEN LIMITATION ADAPTATION
(NLA) is localized at the plasma membrane and was
demonstrated to mediate the ubiquitination of PHT1;1,
likely inducing its CME (Lin et al., 2013). Mutation of
NLA causes high Pi accumulation in plants due to increased PHT1 transporter levels, highlighting the importance of ubiquitin-mediated endocytosis in the regulation
of phosphate uptake.
Thus far, plant membrane transport proteins have
been mainly demonstrated to be internalized using CME;
however, the importance of the clathrin-independent
pathways is only emerging. Single-molecule analysis indeed demonstrated that PIP2;1 is internalized using both
a clathrin-dependent and a membrane raft-associated
pathway involving Flotillin1 (Li et al., 2011).
Recycling of membrane transport proteins from the
EE/TGN to the cell surface appears as a widespread
phenomenon in plants, as illustrated by the accumulation
in BFA bodies of transporters such as PHT1;1, IRT1, and
the boron transporters BOR1 and BOR2, or the water
channel PIP2;1 (Takano et al., 2005; Dhonukshe et al.,
2007; Barberon et al., 2011; Bayle et al., 2011; Miwa et al.,
2013). However, the identity of the ARF-GEFs required
for the recycling of these membrane transport proteins
remains an open question.
Sorting at the MVB: Vacuolar Targeting or Recycling
Ubiquitination constitutes an essential signal to sort
endocytosed membrane proteins in the MVB and to
trigger vacuolar targeting. The boron transporter BOR1
is mono- or diubiquitinated, likely on Lys590, and mutation of this residue to Ala blocks the vacuolar degradation of BOR1 (Kasai et al., 2011). Pharmacological
approaches showed that ubiquitination is not involved in
BOR1 internalization from the plasma membrane but is
rather essential for sorting in the MVB (Fig. 2C; Kasai
et al., 2011). How BOR1 is selected in the MVB remains
to be determined; however, this mechanism probably
involves the ESCRT complex (Henne et al., 2011).
Similarly to BOR1, the iron transporter IRT1 is targeted
to the vacuole for degradation (Barberon et al., 2011).
Monoubiquitination on K154 and K179 likely controls
the IRT1 internalization step; however, ubiquitination
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Nutrient Transporter Dynamics
of other Lys residues or polyubiquitin chain extensions
may control the sorting in MVBs of IRT1, en route to
the vacuole.
In Arabidopsis, the putative retromer component
SNX1 has been implicated in IRT1 recycling (Ivanov
et al., 2014). Mutation of SNX1 leads to reduced iron
import efficiency in roots and correlates with an enhanced degradation of IRT1. In addition, when IRT1
and SNX1 were transiently expressed in tobacco
(Nicotiana tabacum) leaves, IRT1 and SNX1 partially
colocalized in endosomes. SNX1 therefore appears to
drive the recycling of internalized IRT1 to prevent its
premature degradation (Ivanov et al., 2014). Whether
other transporters found in SNX1-positive endosomes,
such as PHT1;1 (Bayle et al., 2011), are recycled after
retromer recognition remains an open question.
REGULATION OF MEMBRANE TRANSPORT
PROTEIN TRAFFICKING BY ENVIRONMENTAL
AND DEVELOPMENTAL CUES
Nutrients are essential for plant growth and development but are also toxic when present in excess.
Therefore, the regulation of the dynamics of nutrient
transporters by their substrates constitutes an elegant
way to rapidly adjust to nutrient availability. As mentioned above, phosphorylation of PHT1;1 on a specific
Ser residue prevents exit from the ER (Bayle et al., 2011).
Interestingly, phosphoproteomic analysis revealed that
Ser phosphorylations at the C terminus of PHT1;1 were
less frequent when plants were grown under phosphate
starvation. The authors proposed that phosphorylation
of Ser residues in PHT1;1 impairs the recognition of a
proximal ER export motif, thus preventing PHT1;1 exit
from the ER when the internal level of phosphate is
high (Bayle et al., 2011). Under Pi-sufficient conditions,
ubiquitination of PHT1s at the ER and post-ER levels
also appears as a way to regulate Pi uptake (Huang et al.,
2013). In the presence of Pi, the ubiquitin-conjugating E2
enzyme PHO2 accumulates and participates in PHT1
ubiquitination, and consequently enhances the degradation of these transporters (Huang et al., 2013). However,
whether PHT1s are degraded by an ERAD process
involving the proteasome or in the vacuole remains
unclear. Indeed, contradictory results have been obtained concerning the sensitivity of PHT1 degradation
to MG132, a well-known inhibitor of the proteasome
(Huang et al., 2013; Park et al., 2014). In addition to
controlling PHT1 exit from the ER, phosphate nutrition
modulates PHT1 endocytosis. Under Pi-sufficient conditions, PHT1;1 undergoes ubiquitin-dependent and
NLA-mediated endocytosis and degradation in the
vacuole (Lin et al., 2013). Interestingly, NLA expression
itself is posttranscriptionally repressed by microRNA827
that is induced by Pi deprivation, adding another level of
regulation by phosphate nutrition.
Boron-induced endocytosis of Arabidopsis BOR1
also represents a good example of substrate-induced
endocytosis. Under boron limitation, BOR1 is localized
at the plasma membrane, where it allows boron radial
transport to vascular tissues. Upon higher boron availability, BOR1 is rapidly endocytosed and targeted to
the vacuole for degradation (Takano et al., 2005). The
Tyr-based motifs located in the large loop of BOR1
are not required for internalization from the plasma
membrane under high boron, but rather allow the recruitment of BOR1 toward an EE/TGN subcompartment
that becomes/fuses with the MVBs (Takano et al., 2010).
In addition, boron excess induces BOR1 ubiquitination,
which in turn accelerates MVB sorting and vacuolar
targeting (Kasai et al., 2011).
The endocytosis of the broad spectrum metal transporter IRT1 is not regulated by the availability of its
primary substrate iron (Barberon et al., 2011). However,
the non-iron metal substrates of IRT1 (zinc, manganese,
and cobalt) were very recently shown to regulate IRT1
dynamics between the EE/TGN and the cell surface
(Barberon et al., 2014). Upon depletion of zinc, manganese, and cobalt, IRT1 relocalizes from the EE/TGN
to the outer polar plasma membrane domain facing
the rhizosphere. Interestingly, the nonubiquitinable
IRT1K154RK179R was found at the plasma membrane in
the presence of metals, providing evidence that the
response to secondary substrates of IRT1 may be mediated by ubiquitination (Barberon et al., 2014). In
Arabidopsis root cells, the early effect of ammonium
excess on the dynamics of the ammonium transporter
AMT1;3 at the plasma membrane was recently investigated by using single-particle approaches (Wang et al.,
2013). Upon ammonium excess, AMT1;3 proteins are
amassed into clusters before being internalized mainly
by CME. Whether this cluster formation of transporters
in response to nutrient excess represents a general
mechanism remains to be clarified in the future.
The relocalization of membrane transport proteins
in response to environmental changes allows plants to
adjust growth and development in their ever-changing
environment. In Arabidopsis, salt stress triggers a
strong inhibition of the root hydraulic conductivity and
concomitantly induces the accumulation of PIP2;1 in
intracellular vesicular structures in root cells (Boursiac
et al., 2005, 2008). Single-molecule analysis demonstrated that under salt stress, the internalization of
PIP2;1 from the plasma membrane involving a clathrinindependent membrane raft-associated pathway was
enhanced (Li et al., 2011). Fluorescence recovery after
photobleaching approaches revealed that salt treatment
also enhanced the cycling of PIP2;1 in Arabidopsis roots
(Luu et al., 2012). The relocalization mechanism of plant
aquaporins is not restricted to PIPs, because Tonoplast
Intrinsic Proteins1;1 were relocalized into putative
intravacuolar invaginations in response to sodium
chloride treatment (Boursiac et al., 2005).
Internalization is also controlled by endogenous
cues and serves developmental programs and adaptation to environmental conditions. Notably, CME is
regulated by several plant hormones, likely reflecting
extensive cross talk between different pathways involved in sorting decisions. Salicylic acid and auxin
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were found to repress the endocytosis of different
cell surface proteins including the aquaporin PIP2;1
(Paciorek et al., 2005; Du et al., 2013).
POLARIZATION OF MEMBRANE TRANSPORT
PROTEINS IN PLANT ROOTS
To properly ensure their physiological function in
root cells, some membrane transport proteins must be
polarly localized. Several nutrient transporters have
been shown to display a lateral polarity in root cells,
with a specific enrichment at the outer or inner plasma
membrane domains. In Arabidopsis, boron uptake
from the soil is performed by the boric acid channel
Nodulin26-like Intrinsic Protein5;1 (NIP5;1) that is
localized at the outer domain of plasma membrane in
root epidermal cells (Takano et al., 2010). By contrast,
the borate exporter BOR1 localizes to the inner domain
of root endodermis cells but also to other cell types
(Takano et al., 2010). The opposite polarity of NIP5;1
and BOR1 is thought to facilitate the transcellular
transport of boron from the rhizosphere to the vascular
tissue of the root. Similarly, the boric acid channel
OsNIP3;1 and OsBOR1, a close ortholog of AtBOR1,
might allow boron transport across the root in rice
(Fuji et al., 2009). Interestingly, Arabidopsis BOR4 is a
borate exporter that is found at the outer domain of the
plasma membrane in root epidermal cells and that
mediates the extrusion of boron from the root, likely to
avoid boron toxicity (Miwa et al., 2007). In rice, cell
polarity is also essential for silicon transport across the
root. This mechanism implies the Low silicon rice1
silicon influx channel and the Low silicon rice2 silicon
exporter that are localized to the outer plasma membrane domain and the inner plasma membrane domain
of the same root cells, respectively (Ma et al., 2006,
2007). In the absence of its secondary substrates, the
iron transporter IRT1 is localized at the outer polar
domain of the plasma membrane of root epidermal cells
(Barberon et al., 2014). This polar localization of IRT1 is
likely critical for proper radial transport of iron and
metals in the root; however whether a polarly localized
metal transporter is found at the inner plasma membrane domain of root epidermal cells is still unknown.
The mechanisms driving the polar localization of
membrane proteins have been mostly described for
PIN-FORMED (PIN) proteins (for review, see Dettmer
and Friml, 2011; Luschnig and Vert, 2014). However,
nutrient transporters now emerge as very interesting
models to study cell polarity in plants, and its functional outcome. Mutation of Tyr-based motifs in BOR1
leads to loss of polarity, showing that these motifs are
important to maintain BOR1 polarity (Takano et al.,
2010). Similar to PIN proteins that are secreted nonpolarly
and then targeted to polar domains by endocytosis and
recycling (Dhonukshe et al., 2008), the authors proposed that BOR1 polarity would be, at least in part,
determined by a recycling-based mechanism requiring
the Tyr-based motifs. Moreover, the lateral diffusion of
BOR1 in the plasma membrane was sufficiently slow to
allow polar localization by such a process (Takano et al.,
2010). In contrast with BOR1, IRT1 polarity is not established by a recycling process involving CME because
IRT1 polar localization is unchanged in presence of a
dominant-negative form of clathrin (Barberon et al., 2014).
Moreover, IRT1 polarity is independent of ubiquitination
because the nonubiquitinable IRT1K154RK179R form is still
localized to the outer plasma membrane domain. Interestingly, IRT1 interacts with the endosome-recruited
FYVE1 protein that controls its localization and polarity
(Barberon et al., 2014). Plants overexpressing FYVE1 accumulate IRT1 at the cell surface in a nonpolar fashion.
Surprisingly, such plants show hypersensitivity to
low iron and decreased metal uptake. This contrasts
greatly with the scenario in which the loss of IRT1
ubiquitination triggers constitutive outer plasma membrane domain localization and correlates with metal
overaccumulation (Barberon et al., 2011). This demonstrates that polarization of IRT1 is critical for proper
radial transport of iron in roots and suggests that iron
exits the root epidermis using efflux transporters rather
than plasmodesmata. This is consistent with old observations that root epidermal cells are symplasmically
isolated (Duckett et al., 1994). In contrast with BOR1
and IRT1 that require recycling mechanisms to be
polarly localized, BOR4 polarity was proposed to be
directly achieved by a polar secretion (Langowski et al.,
2010). Similarly, Medicago truncatula phosphate transporter MtPT4, which is essential for symbiotic phosphate transport and for maintenance of the symbiosis, is
polarly targeted by a mechanism that involves transient
changes in the secretory system of the colonized root
cells (Pumplin et al., 2012).
CONCLUSION
The mechanisms of plant plasma membrane protein
trafficking are heavily influenced by studies on the
auxin efflux carrier PINs. Nutrient transporters and water
channels recently emerged as very interesting models to
further study plant membrane protein dynamics. Altogether, they offer the possibility to grasp the mechanisms
driving plant membrane protein trafficking and how
developmental and environmental cues affect their subcellular dynamics to adjust to ever-changing growth
conditions. A better understanding of the regulatory
mechanisms controlling nutrient transporters and channels may provide biotechnological targets for crop improvement to rationalize fertilizer usage and to achieve
better use of arable land. The knowledge gained over
the past decade on plant membrane transport proteins
brought to light the similarities and differences in membrane protein sorting strategies and therefore offered an
evolutionary perspective on membrane protein trafficking. Plant membrane protein trafficking, which greatly
suffered over the years from excessive homology-based
comparisons with yeast and mammalian cells, can now
be considered as an exciting field of research by itself.
506
Plant Physiol. Vol. 166, 2014
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Copyright © 2014 American Society of Plant Biologists. All rights reserved.
Nutrient Transporter Dynamics
ACKNOWLEDGMENTS
We apologize to colleagues whose work could not be cited due to space
constraints.
Received June 3, 2014; accepted July 14, 2014; published July 17, 2014.
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